Review
How understanding aboveground–belowground linkages can assist restoration ecology

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The topic of aboveground–belowground linkages has seen much recent activity, resulting in several conceptual advances regarding plant–soil feedbacks, multitrophic interactions, and how organisms drive ecosystem processes. Although restoration ecology has been rapidly evolving as a scientific discipline, the principles that have developed regarding aboveground–belowground linkages have yet to be thoroughly integrated into it. In this review, we conceptually integrate the role of aboveground–belowground linkages with the principles of restoration ecology through a framework that transcends multiple levels of ecological organization, and illustrate its application through three examples: restoration of abandoned land, reversal of biological invasions, and restoration of natural disturbances. We conclude that this integration can greatly assist restoration ecology, through aiding identification of effective invention practices and prediction of ecosystem recovery.

Section snippets

The linking of two emerging fields of research

Terrestrial ecosystems are comprised of two distinct components or compartments, one aboveground and the other belowground. The role of interactions between these two components in driving community and ecosystem properties is an emerging area of research which has seen several conceptual advances over the past decade 1, 2, 3, 4, 5. As a result, there is increasing recognition that aboveground and belowground components of ecosystems are strongly linked through a variety of both direct and

Conceptual framework

Ecological restoration can either follow a holistic approach through focusing on the disturbed ecosystem ‘as a whole’, or a more targeted approach concentrating on particular ecosystem components or properties. Effective implementation of either approach requires a full understanding of aboveground–belowground linkages across multiple levels of ecological organization. Here, we present a conceptual framework (Box 1) which is based on explicit recognition that (1) interventions during

Restoration of degraded and abandoned lands

Restoration of (semi-)natural ecosystems after cessation of human land use such as mining and agriculture is frequently performed to aid biodiversity conservation [62]. Consideration of aboveground–belowground linkages can inform intervention practices guiding the successional development towards the historical (or desired) ecosystem state, as has been shown for the restoration of species-rich grasslands on ex-arable land (Box 2). Inter-dependent groups of organisms may differ greatly in their

Conclusions

Counteracting human-induced transformation and degradation of natural ecosystems necessitates active ecological restoration and intervention. Although many questions remain unanswered (Box 4), there have been significant recent advances in our understanding of the links and feedbacks between the aboveground and belowground subsystems, and this in turn has great potential to advance the field of restoration ecology. As we illustrate through our conceptual framework (Box 1) and three examples,

Acknowledgements

We thank Gerlinde De Deyn, Wim van der Putten, and two anonymous reviewers for helpful comments on earlier drafts of this manuscript.

References (100)

  • J. Van Dijk

    Can differences in soil community composition after peat meadow restoration lead to different decomposition and mineralization rates?

    Soil Biol. Biochem.

    (2009)
  • P. Kardol

    Restoration of species-rich grasslands on ex-arable land: Seed addition outweighs soil fertility reduction

    Biol. Conserv.

    (2008)
  • V.A. Cramer

    What's new about old fields? Land abandonment and ecosystem assembly

    Trends Ecol. Evol.

    (2008)
  • C.H. Watts

    Rapid beetle community convergence following experimental habitat restoration in a mined peat bog

    Biol. Conserv.

    (2008)
  • R. Lal

    Soil carbon sequestration to mitigate climate change

    Geoderma

    (2004)
  • L.A. Biederman

    Nematode community development early in ecological restoration: The role of organic amendments

    Soil Biol. Biochem.

    (2008)
  • S. Boyer et al.

    The potential of earthworms to restore ecosystem services after opencast mining – A review

    Basic Appl. Ecol.

    (2010)
  • W.J. Bond et al.

    Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems

    Trends Ecol. Evol.

    (2005)
  • R.L. Beschta et al.

    Large predators and trophic cascades in terrestrial ecosystems of the western United States

    Biol. Conserv.

    (2009)
  • R.D. Bardgett et al.

    Herbivore-mediated linkages between aboveground and belowground communities

    Ecology

    (2003)
  • D.A. Wardle

    Ecological linkages between aboveground and belowground biota

    Science

    (2004)
  • Van der Heijden, M.G.A. et al. (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity...
  • W.H. Van der Putten

    Empirical and theoretical challenges in aboveground-belowground ecology

    Oecologia

    (2009)
  • J. Hines

    Nutrient subsidies to belowground microbes impact aboveground food web interactions

    Ecology

    (2006)
  • I. Kaplan

    Field evidence for indirect interactions between foliar-feeding insect and root-feeding nematode communities on Nicotiana tabacum

    Ecol. Entomol.

    (2009)
  • G.B. De Deyn

    Above- and belowground insect herbivores differentially affect soil nematode communities in species-rich plant communities

    Oikos

    (2007)
  • M.G.A. Van der Heijden et al.

    Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems

    J. Ecol.

    (2009)
  • J.D. Hoeksema

    A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi

    Ecol. Lett.

    (2010)
  • C. Fortunel

    Leaf traits capture the effects of land use changes and climate on litter decomposability of grasslands across Europe

    Ecology

    (2009)
  • F.P. Teste

    Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer

    Ecology

    (2009)
  • T.P. Young

    The ecology of restoration: historical links, emerging issues and unexplored realms

    Ecol. Lett.

    (2005)
  • R.J. Hobbs et al.

    Towards a conceptual framework for restoration ecology

    Restor. Ecol.

    (1996)
  • M.A. Palmer

    Ecological theory and community restoration ecology

    Restor. Ecol.

    (1997)
  • V.T. Eviner et al.

    Embracing variability in the application of plant-soil interactions to the restoration of communities and ecosystems

    Restor. Ecol.

    (2008)
  • R.F. Pywell

    Enhancing diversity of species-poor grasslands: an experimental assessment of multiple constraints

    J. Appl. Ecol.

    (2007)
  • L.R. Walker et al.

    Lessons from primary succession for restoration of severely damaged habitats

    Appl. Veg. Sci.

    (2009)
  • D.A. Wardle et al.

    Human-induced changes in large herbivorous mammal density: the consequences for decomposers

    Front. Ecol. Environ.

    (2004)
  • T. Fukami

    Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems

    Ecol. Lett.

    (2006)
  • D.R. Towns

    Predation of seabirds by invasive rats: multiple indirect consequences for invertebrate communities

    Oikos

    (2009)
  • K. Birkhofer

    Subsidy from the detrital food web, but not microhabitat complexity, affects the role of generalist predators in an aboveground herbivore food web

    Oikos

    (2008)
  • E.J. Fichtner

    Survival, dispersal, and potential soil-mediated suppression of Phytophthora ramorum in a California redwood-tanoak forest

    Phytopathology

    (2009)
  • K.O. Reinhart

    Plant-soil biota interactions and spatial distribution of black cherry in its native and invasive ranges

    Ecol. Lett.

    (2003)
  • R.M. Callaway

    Soil biota and exotic plant invasion

    Nature

    (2004)
  • A.M. Piskiewicz

    Soil microorganisms control plant ectoparasitic nematodes in natural coastal foredunes

    Oecologia

    (2007)
  • B.E. Wolfe et al.

    Breaking new ground: Soil communities and exotic plant invasion

    Bioscience

    (2005)
  • B.S. Richter et al.

    Mycorrhizal inoculation of big sacaton: Implications for grassland restoration of abandoned agricultural fields

    Restor. Ecol.

    (2002)
  • J. Koricheva

    Effects of mycorrhizal fungi on insect herbivores: a meta-analysis

    Ecology

    (2009)
  • M.L. Forup

    The restoration of ecological interactions: plant-pollinator networks on ancient and restored heathlands

    J. Appl. Ecol.

    (2008)
  • J. Bascompte

    Mutualistic networks

    Front. Ecol. Environ.

    (2009)
  • Cited by (0)

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